Unidirectional Movement of Cellulose Synthase Complexes in Arabidopsis Seed Coat Epidermal Cells Deposit Cellulose Involved in Mucilage Extrusion, Adherence, and Ray Formation

• Published in: Plant physiology (Bethesda) 2015-06, Vol.168 (2), p.502-520
• Main Authors: Griffiths, Jonathan S., Šola, Krešimir, Kushwaha, Rekha, Lam, Patricia, Tateno, Mizuki, Young, Robin, Voiniciuc, Cǎtǎlin, Dean, Gillian, Mansfield, Shawn D., DeBolt, Seth, Haughn, George W.
• Format: Article
• Language: English
• Subjects: American culture; Amino Acid Sequence; Arabidopsis; Arabidopsis - enzymology; Arabidopsis Proteins - chemistry; Arabidopsis Proteins - metabolism; Biology; Biosynthesis; CELL BIOLOGY; Cell walls; cellulose; Cellulose - metabolism; cellulose synthase; Cytoplasm - metabolism; Epidermal cells; extrusion; Genetic mutation; Glucosyltransferases - chemistry; Glucosyltransferases - metabolism; Green Fluorescent Proteins - metabolism; Life Sciences; Microtubules; Microtubules - metabolism; Models, Biological; Molecular Sequence Data; Multienzyme Complexes - metabolism; Mutation - genetics; Pectins - metabolism; Plant Epidermis - cytology; Plant Mucilage - metabolism; Plants; Protein Binding; Protein Structure, Tertiary; Proteins; seed coat; Seeds - cytology; Testa; Zinc Fingers
• ISSN: 0032-0889; 1532-2548
• DOI: 10.1104/pp.15.00478

CELLULOSE SYNTHASE5 (CESA5) synthesizes cellulose necessary for seed mucilage adherence to seed coat epidermal cells of Arabidopsis (Arabidopsis thaliana). The involvement of additional CESA proteins in this process and details concerning the manner in which cellulose is deposited in the mucilage pocket are unknown. Here, we show that bothCESA3andCESA10are highly expressed in this cell type at the time of mucilage synthesis and localize to the plasma membrane adjacent to the mucilage pocket. Theisoxaben resistant1-1andisoxaben resistant1-2mutants affectingCESA3show defects consistent with altered mucilage cellulose biosynthesis. CESA3 can interact with CESA5 in vitro, and green fluorescent protein-tagged CESA5, CESA3, and CESA10 proteins move in a linear, unidirectional fashion around the cytoplasmic column of the cell, parallel with the surface of the seed, in a pattern similar to that of cortical microtubules. Consistent with this movement, cytological evidence suggests that the mucilage is coiled around the columella and unwinds during mucilage extrusion to form a linear ray. Mutations inCESA5andCESA3affect the speed of mucilage extrusion and mucilage adherence. These findings imply that cellulose fibrils are synthesized in an ordered helical array around the columella, providing a distinct structure to the mucilage that is important for both mucilage extrusion and adherence.